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Sébastian LEQUIME UNIVERSITÉ PIERRE ET MARIE CURIE ECOLE DOCTORALE 515 « Complexité du Vivant » Groupe à 5 ans – Interactions Virus-Insectes Interactions flavivirus – moustiques : diversité et transmission ! par Sébastian LEQUIME THÈSE DE DOCTORAT en EVOLUTION VIRALE Présentée et soutenue publiquement le : 21 Juin 2016 Devant un jury composé de : M. Samuel ALIZON, Chargé de Recherche Rapporteur M. Jacob KOELLA, Professeur Rapporteur M. Dominique HIGUET, Professeur Examinateur Mme Anna-Bella FAILLOUX, Directeur de Recherche Examinatrice M. Serafín GUTIERREZ, Chargé de Recherche Examinateur M. Louis LAMBRECHTS, Chargé de Recherche Directeur de thèse « Je sais qu’au point où en est arrivée aujourd’hui la microbiologie, tout nouveau grand pas en avant sera une affaire des plus pénibles et que l’on aura beaucoup de mécomptes et de déceptions. » – Alexandre YERSIN, 28 août 1891. Résumé Les infections humaines dues aux virus du genre Flavivirus constituent depuis longtemps un problème de santé publique majeur à travers le monde, en particulier dans les zones à climat tropical. Ces virus à ARN sont des arbovirus qui infectent alternativement un hôte vertébré et un arthropode « vecteur », dont majoritairement des moustiques de la sous-famille des Culicinae. D’autres flavivirus, en revanche, sont incapables d’infecter les cellules de vertébrés et sont qualifiés de flavivirus spécifiques d’insectes (FSI). L’interaction entre les vecteurs et les flavivirus est centrale dans leur biologie, par l’influence qu’elle a sur leur diversité génétique, leur évolution et leur transmission. Cependant, après plus d’un siècle de recherches scientifiques, certains points de ces aspects fondamentaux restent méconnus, malgré une abondance accrue de données. Les approches basées sur les « mégadonnées » (big data) ont été au cœur du travail de cette thèse, qu’elles aient été générées par des technologies modernes ou par compilation de travaux plus anciens. Dans une première partie, nous avons exploré des génomes de moustiques ano- phèles disponibles dans les bases de données publiques, à la recherche de traces d’éléments viraux endogènes (EVEs) d’origine flavivirale. Nous avons réussi à identi- fier in silico, puis à confirmer in vivo, la présence d’EVEs proches des FSI exogènes, chez les espèces Anopheles sinensis et An. minimus. Ces résultats suggèrent l’existence de FSI chez les anophèles, habituellement non associés aux , et mettent en lumière la diversité du genre Flavivirus, loin d’être restreinte aux seuls arbovirus. Dans une deuxième partie, nous avons généré et analysé un jeu de données com- plexe basé sur le séquençage haut-débit d’un flavivirus à l’intérieur de son vecteur. Cette étude nous a permis d’explorer la fine interaction entre le génotype du mous- tique Aedes aegypti et la diversité virale intra-hôte du virus de la dengue-1. En effet, v Résumé comme tous les virus à ARN, les flavivirus existent sous la forme d’une population de variants génétiques apparentés, considérée comme critique pour leur fitness et leur potentiel adaptatif. Nos résultats ont mis en évidence : (i) un fort effet de la dérive génétique liée à un goulot d’étranglement démographique lors de l’infection initiale du tube digestif, diminuant l’importance relative de la sélection naturelle, et (ii) une modulation de la diversité génétique intra-hôte du virus par le génotype du mous- tique, indiquant que la diversité génétique du virus, et donc sa fitness et son évolution, est inextricablement liée à la variation génétique de l’hôte. Enfin, nous avons compilé de manière systématique la riche littérature disponible sur la transmission verticale des arbovirus chez le vecteur moustique, c’est-à-dire de la femelle infectée à sa descendance, afin d’identifier des facteurs techniques, environ- nementaux, taxonomiques et physiologiques sous-jacents. Nos résultats, étayés par une analyse statistique robuste, éclairent d’un jour nouveau ce mode de transmission complémentaire à la transmission horizontale, entre le vecteur et l’hôte vertébré. Ils permettent d’affiner notre compréhension des stratégies employées par les arbovirus pour persister dans leur environnement, tout en fournissant des hypothèses testables sur les processus biologiques impliqués. Collectivement, nos résultats ont mis en évidence de nouveaux aspects de la com- plexité des relations entre flavivirus et moustiques. Au-delà, ils soulignent l’intérêt d’étudier les « mégadonnées » générées au cours de plus d’un siècle de recherche, qu’elles soient issues de l’accumulation historique d’études descriptives ou produites par les technologies récentes de séquençage haut-débit. Ces analyses inscrivent réso- lument l’étude du système flavivirus-moustique dans l’ère du big data. vi Abstract Human infections caused by members of the Flavivirus genus have long been a major public health burden worldwide, especially in tropical climates. These RNA vi- ruses are arboviruses that infect alternatively vertebrate hosts and arthropod ‘vectors’, mainly mosquitoes in the Culicinae subfamily. Other flaviviruses, however, are unable to infect vertebrate cells and are accordingly called insect-specific flaviviruses (ISFs). The interaction between vectors and flaviviruses is key to understanding their biology, because it influences their genetic diversity, evolution and transmission. Despite more than a century of scientific research and an ever-increasing amount of data, some fundamental aspects are still poorly understood. Strategies based on ‘big data’ have been at the heart of the work presented in this dissertation, both by taking advantage of modern technologies and by compiling older literature. In the first part, we explored publicly available Anopheles mosquito genomes to discover putative endogenous viral elements (EVEs) of flaviviral origin. We identified in silico and confirmed in vivo one EVE in the genome of Anopheles minimus and another in the genome of Anopheles sinensis. Both EVEs were related to exogenous ISFs. These results support the existence of ISFs in Anopheles mosquitoes, which are not usually associated with flaviviruses, and highlight the diversity of the Flavivirus genus, far from being restricted to arboviruses. In the second part, we generated and analyzed a complex dataset based on deep sequencing of a flavivirus within its vector. This study allowed us to investigate the fine-tuned interaction between genotypes of the mosquito Aedes aegypti and the intra-host diversity of dengue virus 1. Like other RNA viruses, flaviviruses consist of a population of related genetic variants, which is considered critical for their fitness vii Abstract and adaptive potential. Our results showed : (i) a strong effect of genetic drift due to a population bottleneck during initial infection of the digestive tract, reducing the relative importance of natural selection, and (ii) a modulation of the intra-host viral genetic diversity by the mosquito genotype, indicating that viral genetic diversity, and therefore virus fitness and evolution, is inextricably linked to host genetic variation. In the last part, we conducted a systematic review of the abundant literature on arbovirus vertical transmission in the mosquito vector, i.e. from an infected female to her offspring, in order to identify technical, environmental, taxonomic and phy- siological predictors. Our results, based on a robust statistical framework, shed new light on this transmission mode, complementary to horizontal transmission between the vector and the vertebrate host. They contribute to refining our understanding of strategies employed by arboviruses to persist in their environment, while providing testable hypotheses about the underlying biological processes. Collectively, our results highlight new aspects of the complex relationships bet- ween flaviviruses and mosquitoes. Moreover, they underline the new insights brought by the ‘big data’ compiled during more than one century of research, either extracted from historical, descriptive studies or generated by modern, high-throughput se- quencing technologies. Such analyses clearly include the study of flavivirus-mosquito systems in the era of ‘big data’. viii Remerciements Mes premiers remerciements vont à Louis LAMBRECHTS. Merci d’avoir accepté de diriger ma thèse. J’ai beaucoup appris à ton contact, que ce soit en biologie évolu- tive/écologie, en statistiques, ou sur la vie scientifique en général. Merci également de m’avoir fait confiance et laissé évoluer à mon propre rythme. C’est grâce à ton encadrement que je me sens prêt aujourd’hui à voler de mes propres ailes et qui sait, à peut-être envisager sérieusement une carrière de recherche académique. Je souhaite sincèrement remercier les rapporteurs, Samuel ALIZON et Jacob KOELLA, ainsi que les autres membres du jury, Anna-Bella FAILLOUX, Dominique HIGUET et Serafín GUTIERREZ, d’avoir accepté d’évaluer dans le détail mon travail. Merci également à tous les membres de l’IVI, passés et présents. Plus que des collègues, ce sont des amis très chers que j’ai trouvés au 4ème étage du Centre François Jacob. Ces trois années sont passées trop vite, tant votre dynamisme, l’entraide et la bonne ambiance que nous avons instauré m’ont permis d’affronter sereinement cette thèse : • Catherine, je ne sais vraiment pas ce que nous ferions sans ton aide au quoti- dien ; • Albin, pour avoir supporté tant bien que mal mes incessantes allées et venues dans ton bureau, et pour avoir piqué en moi ce petit désir de compétition qui m’a fait apprendre à utiliser couramment R, les stats, la bioinfo et m’a fait tant peaufiner mes figures
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